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Assessment of the lipid production potential of six benthic diatom species grown in airlift photobioreactors

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Abstract

In recent years diatoms have emerged as a major algal source for the production of bioactive compounds. Marine diatoms grow quickly and can store high amount of lipids. Unfortunately, they are little studied and underexploited resources. The current work deals with an original and rarely investigated source of diatoms: intertidal mudflats. It aims to evaluate the lipid production potential of some strains of benthic diatom species, isolated and hosted in the Nantes Culture Collection (NCC) when cultivated in an airlift photobioreactor. Six strains known for their high biomass and/or lipid productivity: Amphora sp. (NCC169), Entomoneis paludosa (NCC18.2), Nitzschia alexandrina (NCC33), Nitzschia sp. (NCC109), Opephora sp. (NCC366), and Staurosira sp. (NCC182) were cultivated in airlift photobioreactors for the first time. Their lipid class composition, fatty acid, and sterol distribution were studied. Total lipid production varied from 11.4 (Amphora sp.) to 41%DW (Staurosira sp.). Neutral lipid amounts varied from 23 (Amphora sp.) to 76% (Staurosira sp.) of total lipids (%TL). Glycolipids ranged from 18 (Staurosira sp.) to 59%TL (Opephora sp.) and phospholipids accounted for 6 (Staurosira sp.) to 26%TL (Amphora sp.). Some qualitative and quantitative differences were identified in both fatty acid and sterol composition in the different strains analyzed. Staurosira sp. seems to be the most promising species in terms of lipid production and most particularly in triacylglycerol production. Entomoneis paludosa produced phytosterols and eicosapentaenoic acid (EPA), compounds with potential for application in the pharmaceutical sector. Nitzschia alexandrina produced squalene and low levels of saturated fatty acids which could both be interesting in the nutraceutical industry as antioxidants.

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References

  • Achitouv E, Metzger P, Rager M-N, Largeau C (2004) C31-C34 methylated squalenes from a Bolivian strain of Botryococcus braunii. Phytochemistry 65:3159–3165

    Article  CAS  PubMed  Google Scholar 

  • Artamonova EY, Svenning JB, Vasskog T, Hansen E, Eilertsen HC (2017) Analysis of phospholipids and neutral lipids in three common northern cold water diatoms: Coscinodiscus concinnus, Porosira glacialis, and Chaetoceros socialis, by ultra-high performance liquid chromatography-mass spectrometry. J Appl Phycol 29:1241–1249

    Article  CAS  Google Scholar 

  • Barrett SM, Volkman JK, Dunstan GA, LeRoi J (1995) Sterols of 14 species of marine diatoms (Bacillariophyta). J Phycol 31:360–369

    Article  CAS  Google Scholar 

  • Bergé J-P, Barnathan G (2005) Fatty acids from lipids of marine organisms: molecular biodiversity, roles as biomarkers, biologically active compounds, and economical aspects. Adv Biochem Eng Biotechnol 96:49–125

    PubMed  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  PubMed  Google Scholar 

  • Blunt JW, Copp BR, Munro MH, Northcote PT, Prinsep MR (2011) Marine natural products. Nat Prod Rep 28:196–268

    Article  CAS  PubMed  Google Scholar 

  • Borowitzka MA (2013) High-value products from microalgae—their development and commercialisation. J Appl Phycol 25:743–756

    Article  CAS  Google Scholar 

  • Chen Y-C (2012) The biomass and total lipid content and composition of twelve species of marine diatoms cultured under various environments. Food Chem 131:211–219

    Article  CAS  Google Scholar 

  • Chew KW, Yap JY, Show PL, Suan NH, Juan JC, Ling TC, Lee D-J, Chang J-S (2017) Microalgae biorefinery: high value products perspectives. Bioresour Technol 229:53–62

    Article  CAS  PubMed  Google Scholar 

  • Chuecas L, Riley JP (1969) Component fatty acids of the total lipids of some marine phytoplankton. J Mar Biol Assoc U K 49:97–116

    Article  CAS  Google Scholar 

  • Cointet E, Wielgosz-Collin G, Méléder V, Gonçalves O (2019a) Lipids in benthic diatoms: a new suitable screening procedure. Algal Res 39:101425

    Article  Google Scholar 

  • Cointet E, Wielgosz-Collin G, Bougaran G, Rabesaotra V, Gonçalves O, Méléder V (2019b) Effects of light and nitrogen availability on photosynthetic efficiency and fatty acid content of three original benthic diatom strains. PLoS One 14:e0224701

  • da Costa E, Melo T, Moreira A, Bernardo C, Helguero L, Ferreira I, Cruz M, Rego A, Domingues P, Calado R, Abreu M, Domingues MR (2017) Valorization of lipids from Gracilaria sp. through lipidomics and decoding of antiproliferative and anti-inflammatory activity. Mar Drugs 15:62

    Article  PubMed Central  CAS  Google Scholar 

  • de Castro AS, Garcia V (2005) Growth and biochemical composition of the diatom Chaetoceros cf. wighamii brightwell under different temperature, salinity and carbon dioxide levels. I. Protein, carbohydrates and lipids. Aquaculture 246:405–412

    Article  CAS  Google Scholar 

  • Dunstan GA, Volkman JK, Barrett SM, Leroi J-M, Jeffrey SW (1993) Essential polyunsaturated fatty acids from 14 species of diatom (Bacillariophyceae). Phytochemistry 35:155–161

    Article  Google Scholar 

  • Fernández FA, Perez JS, Sevilla JF, Camacho FG, Grima EM (2000) Modeling of eicosapentaenoic acid (EPA) production from Phaeodactylum tricornutum cultures in tubular photobioreactors. Effects of dilution rate, tube diameter, and solar irradiance. Biotechnol Bioeng 68:173–183

    Article  PubMed  Google Scholar 

  • Geng H-X, Yu R-C, Chen Z-F, Peng Q-C, Yan T, Zhou M-J (2017) Analysis of sterols in selected bloom-forming algae in China. Harmful Algae 66:29–39

    Article  CAS  PubMed  Google Scholar 

  • Gladu PK, Patterson GW, Wikfors GH, Chitwood DJ, Lusby W (1991) Sterols of some diatoms. Phytochemistry 30:2301–2303

    Article  CAS  Google Scholar 

  • Granum E, Myklestad SM (2002) A photobioreactor with pH control: demonstration by growth of the marine diatom Skeletonema costatum. J Plankton Res 24:557–563

    Article  CAS  Google Scholar 

  • Grossi V, Beker B, Geenevasen JA, Schouten S, Raphel D, Fontaine M-F, Damsté JSS (2004) C25 highly branched isoprenoid alkenes from the marine benthic diatom Pleurosigma strigosum. Phytochemistry 65:3049–3055

    Article  CAS  PubMed  Google Scholar 

  • Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, pp 29-60

  • Hamed I, Özogul F, Özogul Y, Regenstein JM (2015) Marine bioactive compounds and their health benefits: a review. Compr Rev Food Sci Food Saf 14:446–465

    Article  CAS  Google Scholar 

  • Hildebrand M, Davis AK, Smith SR, Traller JC, Abbriano R (2012) The place of diatoms in the biofuels industry. Biofuels 3:221–240

    Article  CAS  Google Scholar 

  • Huntley ME, Johnson ZI, Brown SL, Sills DL, Gerber L, Archibald I, Machesky SC, Granados J, Beal C, Greene CH (2015) Demonstrated large-scale production of marine microalgae for fuels and feed. Algal Res 10:249–265

    Article  Google Scholar 

  • Kendel M, Couzinet-Mossion A, Viau M, Fleurence J, Barnathan G, Wielgosz-Collin G (2013) Seasonal composition of lipids, fatty acids, and sterols in the edible red alga Grateloupia turuturu. J Appl Phycol 25:425–432

    Article  CAS  Google Scholar 

  • Krichnavaruk S, Loataweesup W, Powtongsook S, Pavasant P (2005) Optimal growth conditions and the cultivation of Chaetoceros calcitrans in airlift photobioreactor. Chem Eng J 105:91–98

    Article  CAS  Google Scholar 

  • Krichnavaruk S, Powtongsook S, Pavasant P (2007) Enhanced productivity of Chaetoceros calcitrans in airlift photobioreactors. Bioresour Technol 98:2123–2130

    Article  CAS  PubMed  Google Scholar 

  • Lebeau T, Robert J-M (2003) Diatom cultivation and biotechnologically relevant products. Part II: current and putative products. Appl Microbiol Biotechnol 60:624–632

    Article  CAS  PubMed  Google Scholar 

  • Levitan O, Dinamarca J, Hochman G, Falkowski PG (2014) Diatoms: a fossil fuel of the future. Trends Biotechnol 32:117–124

    Article  CAS  PubMed  Google Scholar 

  • Lukavský J (2000) Vonshak, A. (Ed.): Spirulina platensis (Arthrospira). Physiology, cell biology and biotechnology. Photosynthetica 38:552–552

    Article  Google Scholar 

  • Massé G, Belt ST, Rowland SJ, Rohmer M (2004) Isoprenoid biosynthesis in the diatoms Rhizosolenia setigera (Brightwell) and Haslea ostrearia (Simonsen). Proc Natl Acad Sci 101:4413–4418

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Medina AR, Grima EM, Giménez AG, González MI (1998) Downstream processing of algal polyunsaturated fatty acids. Biotechnol Adv 16:517–580

    Article  CAS  Google Scholar 

  • Molina E, Fernández FA, Camacho FG, Rubio FC, Chisti Y (2000) Scale-up of tubular photobioreactors. J Appl Phycol 12:355–368

    Article  Google Scholar 

  • Monkonsit S, Powtongsook S, Pavasant P (2011) Comparison between airlift photobioreactor and bubble column for Skeletonema costatum cultivation. Engl J 15:53–64

    Article  Google Scholar 

  • Nagao K, Yanagita T (2005) Conjugated fatty acids in food and their health benefits. J Biosci Bioeng 100:152–157

    Article  CAS  PubMed  Google Scholar 

  • Nappo M, Berkov S, Codina C, Avila C, Messina P, Zupo V, Bastida J (2009) Metabolite profiling of the benthic diatom Cocconeis scutellum by GC-MS. J Appl Phycol 21:295–306

    Article  CAS  Google Scholar 

  • Nghiem Xuan R, Safitri I, Mouget JL, Pruvost J, Turpin V, Jaouen P (2020) Design of an artificial culture medium to optimize Haslea ostrearia biomass and marennine production. Algal Res 45:101653

    Article  Google Scholar 

  • Nichols PD, Palmisano AC, Volkman JK, Smith GA, White DC (1988) Occurrence of an isoprenoid C25 diunasaturated alkene and high neutral lipid content in Antractic sea-ice diatom communities. J Phycol 24:90–96

    Article  CAS  Google Scholar 

  • Nichols DS, Nichols PD, Sullivan CW (1993) Fatty acid, sterol and hydrocarbon composition of Antarctic sea ice diatom communities during the spring bloom in McMurdo Sound. Antarct Sci 5:271–278

    Article  Google Scholar 

  • Niu Y-F, Zhang M-H, Li D-W, Yang W-D, Liu J-S, Bai W-B, Li H-Y (2013) Improvement of neutral lipid and polyunsaturated fatty acid biosynthesis by overexpressing a type 2 diacylglycerol acyltransferase in marine diatom Phaeodactylum tricornutum. Mar Drugs 11:4558–4569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plouguerné E, Souza L, Sassaki G, Cavalcanti J, Villela Romanos M, Gama B, Pereira R, Barreto-Bergter E (2013) Antiviral sulfoquinovosyldiacylglycerols (SQDGs) from the Brazilian brown seaweed Sargassum vulgare. Mar Drugs 11:4628–4640

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ponomarenko L, Stonik I, Aizdaicher N, Orlova TY, Popovskaya G, Pomazkina G, Stonik V (2004) Sterols of marine microalgae Pyramimonas cf. cordata (Prasinophyta), Attheya ussurensis sp. nov. (Bacillariophyta) and a spring diatom bloom from Lake Baikal. Comp Biochem Physiol B 138:65–70

    Article  CAS  PubMed  Google Scholar 

  • Pulz O (2001) Photobioreactors: production systems for phototrophic microorganisms. Appl Microbiol Biotechnol 57:287–293

    Article  CAS  PubMed  Google Scholar 

  • Rampen SW, Abbas BA, Schouten S, Damsté JSS (2010) A comprehensive study of sterols in marine diatoms (Bacillariophyta): implications for their use as tracers for diatom productivity. Limnol Oceanogr 55:91–105

    Article  CAS  Google Scholar 

  • Sabia A, Clavero E, Pancaldi S, Rovira JS (2018) Effect of different CO2 concentrations on biomass, pigment content, and lipid production of the marine diatom Thalassiosira pseudonana. Appl Microbiol Biotechnol 102:1945–1954

    Article  CAS  PubMed  Google Scholar 

  • Schnurr PJ, Allen DG (2015) Factors affecting algae biofilm growth and lipid production: a review. Renew Sust Energ Rev 52:418–429

    Article  CAS  Google Scholar 

  • Sharma KK, Schuhmann H, Schenk PM (2012) High lipid induction in microalgae for biodiesel production. Energies 5:1532–1553

    Article  CAS  Google Scholar 

  • Silva-Aciares FR, Riquelme CE (2008) Comparisons of the growth of six diatom species between two configurations of photobioreactors. Aquac Eng 38:26–35

    Article  Google Scholar 

  • Stonik V, Stonik I (2015) Low-molecular-weight metabolites from diatoms: structures, biological roles and biosynthesis. Mar Drugs 13:3672–3709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson G Jr (1996) Lipids and membrane function in green algae. Biochim Biophys Acta-Lipids Lipid Metab 1302:17–45

    Article  Google Scholar 

  • Tredici MR (2004) Mass production of microalgae: photobioreactors. In: Richmond A (ed) Handbook of microalgal Culture. Biotechnology and Applied Phycology. Blackwell Science, Oxford, pp 178–214

    Google Scholar 

  • Viso AC, Marty JC (1993) Fatty acids from 28 marine microalgae. Phytochemistry 34:1521–1533

    Article  CAS  Google Scholar 

  • Volkman JK (2016) Sterols in microalgae. In: Beardall J, Raven JA (eds) Borowitzka MA. The physiology of microalgae, Springer Cham, pp 485–505

  • Volkman JK, Hallegraeff GM (1988) Lipids in marine diatoms of the genus Thalassiosira: predominance of 24-methylenecholesterol. Phytochemistry 27:1389–1394

    Article  CAS  Google Scholar 

  • Volkman JK, Barrett SM, Dunstan GA (1994) C25 and C30 highly branched isoprenoid alkenes in laboratory cultures of two marine diatoms. Org Geochem 21:407–414

    Article  CAS  Google Scholar 

  • Yao Y, Lu Y, Peng K-T, Huang T, Niu Y-F, Xie W-H, Yang W-D, Liu J-S, Li H-Y (2014) Glycerol and neutral lipid production in the oleaginous marine diatom Phaeodactylum tricornutum promoted by overexpression of glycerol-3-phosphate dehydrogenase. Biotechnol Biofuels 7:110

    Article  CAS  Google Scholar 

  • Yao L, Gerde JA, Lee S-L, Wang T, Harrata KA (2015) Microalgae lipid characterization. J Agric Food Chem 63:1773–1787

    Article  CAS  PubMed  Google Scholar 

  • Yi Z, Xu M, Di X, Brynjolfsson S, Fu W (2017) Exploring valuable lipids in diatoms. Front Mar Sci 4:17

  • Zapata M, Rodríguez F, Fraga S, Barra L, Ruggiero MV (2011) Chlorophyll c pigment patterns in 18 species (51 strains) of the genus Pseudo-nitzschia (Bacillariophyceae). J Phycol 47:1274–1280

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors express their sincere thanks to Ms. Raphaëlle Touchard (GEPEA) for support and advice on the utilization of the airlift PBR and to Vony Rabesaotra for GC-MS analyses.

Funding

This work was supported by the regional Atlantic Microalgae research program (AMI) which was funded by the Pays de la Loire region.

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Authors and Affiliations

  1. Université de Nantes, Laboratoire Mer Molécules Santé, EA 2160, BP 92208, F-44322, Nantes, France

    Eva Cointet, Elise Séverin, Aurélie Couzinet-Mossion, Vona Méléder & Gaëtane Wielgosz-Collin

  2. Université de Nantes, GEPEA, UMR CNRS-6144, Bât. CRTT, 37 Boulevard de l’Université, BP406, F-44602, Saint-Nazaire Cedex, France

    Olivier Gonçalves

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  1. Eva Cointet
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  5. Olivier Gonçalves
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  6. Gaëtane Wielgosz-Collin
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Contributions

Eva Cointet and Elise Séverin conducted experiments. Eva Cointet, Elise Séverin, Aurélie Couzinet-Mossion, Vona Méléder, Olivier Gonçalves, and Gaëtane Wielgosz-Collin analyzed and interpreted the data. Vona Méléder, Olivier Gonçalves, and Gaëtane Wielgosz-Collin designed and supervised the research. All the authors drafted the work and/or revised it critically and approved the final version of the manuscript.

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Correspondence to Gaëtane Wielgosz-Collin.

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Cointet, E., Séverin, E., Couzinet-Mossion, A. et al. Assessment of the lipid production potential of six benthic diatom species grown in airlift photobioreactors. J Appl Phycol 33, 2093–2103 (2021). https://doi.org/10.1007/s10811-021-02490-4

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